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n order to breathe, we must continuously contract and relax our respiratory muscles about 30,000 times a day, or a billion times for a lifetime of 90 years. Such extreme demands are not made of any other skeletal muscles. The respiratory muscles move the parts of the chest wall that form the boundaries of the thoracic cavity, either enlarging or contracting its volume and thereby ventilating the lungs. This ventilatory pump is obviously essential for life. The main function of the lung is to exchange gas, whereas the main function of the ventilatory pump is to replenish the alveoli with fresh air and to expel alveolar gas from the lung.
VENTILATORY PUMP
The ventilatory pump consists of the following: (1) the respiratory muscles, which expand and contract the thoracic cavity; (2) the compartments of the chest wall that the muscles displace when they contract, namely the rib cage and abdomen; (3) the cortical and brainstem centers that control the respiratory muscles; and (4) the intervening neural connections. What are the respiratory muscles, and how do they accomplish their task? Ignoring the upper airway muscles, which contract to maintain airway patency, the main respiratory muscles are as follows: (1) the diaphragm, divided into its costal and crural parts, which have different actions, anatomic origins, and cervical segmental innervations1,2; (2) the abdominal muscles, of which the transversus muscle appears to be the most important in breathing3; (3) the inspiratory muscles of the rib cage, including the external intercostal muscles, the parasternal muscles, the scalene muscles, and the sternocleidomastoid muscles47; and (4) the expiratory muscles of the rib cage, including the internal intercostal muscles and the triangularis sterni muscle.8 A complete description of the respiratory muscles can be found
* Modified with permission from Macklem PT. The act of breathing. In: Aliverti A, Brusasco V, Macklem PT, Pedotti A, editors. Mechanics of breathing: pathophysiology, diagnosis and treatment. Milan: Springer-Verlag; 2002. p. 311.
elsewhere in this book (see Chapter 22, Actions of the Respiratory Muscles). The compartments displaced by the respiratory muscles are the rib cage and the abdomen.9 Outward displacements of the abdominal wall and expansion of the rib cage are inspiratory, and vice versa. When these two compartments move in opposite directions, with expansion of one and contraction of the other, there is very little interaction between the two.9,10 However, what interaction there is cannot be ignored,11,12 as is discussed below. A substantial part of the internal surface of the rib cage is directly apposed to the diaphragm.13 As a result, one can model the rib cage as being composed of two subcompartments, the part that is apposed to the lung, the pulmonary rib cage, and the part apposed to the diaphragm, the abdominal rib cage.14 The boundary between the two compartments is at the level of the xiphisternum at functional residual capacity (FRC). Ribs 1 to 6 are tightly attached to the sternum and thus form part of the pulmonary rib cage. Ribs 7 to 12 are loosely attached to the sternum through considerably longer costal cartilages. The parts of them below the level of the xiphisternum form part of the abdominal rib cage.
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Mechanics of Breathing
Probably the most important expiratory rib cage muscle is the triangularis sterni muscle, which originates from the lateral border of the sternum and runs axially and laterally in a cephalad direction to insert into the lower border of the ribs of the pulmonary rib cage.8 The abdominal rib cage is exposed on its inner surface to Ppl over the surface of the diaphragm. This pressure, in contrast to Ppl over the surface of the lung, generally rises during inspiration. This reflects the rise in abdominal pressure (Pab) when the diaphragm contracts and pushes down on the abdominal contents, displacing the abdomen outward. Pab is transmitted through the costal diaphragmatic fibers to the pleural space in the area of apposition and acts to expand the abdominal rib cage.13 In addition, the costal diaphragmatic fibers originate from ribs 7 to 11 and run axially in the area of apposition to insert on the central tendon. Thus, with diaphragmatic contraction there is a cephalad force acting on the abdominal rib cage in concert with Pab to expand it.15,16 The abdominal muscles are also attached to the abdominal rib cage, and when they are recruited, they act to contract it.3 Apart from a small slip of the costal part of the diaphragm attached to the sternum, the diaphragm has no attachments on the pulmonary rib cage and therefore has no direct action on it. Therefore, to a reasonable approximation, the agencies acting on the pulmonary rib cage in the absence of rib cage distortion are Ppl over the surface of the lung and the pressures developed by the rib cage muscles (Prcm). At equilibrium, these agencies must be balanced by the elastic recoil pressure of the pulmonary rib cage (Prc,p): Prc,p Prcm Ppl. In contrast, the agencies acting on the abdominal rib cage in the absence of rib cage distortion are Pab, a fraction of transdiaphragmatic pressure (Pdi Pab Ppl), called the insertional component of Pdi (xPdi, where 1 x 0),1517 and a fraction of the pressure developed by the abdominal muscles (Pabm), called the insertional component of Pabm (yPabm, where 1 y 0).17 At equilibrium, these agencies must be balanced by the elastic recoil of the abdominal rib cage (Prc,a): Prc,a xPdi Pab yPabm (yPabm is given a negative sign because its action is deflationary, whereas xPdi and Pab are inflationary). Although the rib cage can be easily distorted,1820 in quiet breathing and exercise this does not occur to any significant extent.21 Therefore: Prc,p Prc,a Prcm Ppl xPdi Pab yPabm and by rearranging: Prcm (x 1)Pdi yPabm (7-1)
action is primarily on the rib cage, not the abdomen. No abdominal muscles act to expand the abdominal wall. Thus, the caudal part of the abdominal wall always expands passively, either as a result of an increase in abdominal pressure due to diaphragmatic contraction or because of relaxation of abdominal muscle contraction, when abdominal pressure can actually fall during abdominal expansion.17
In a similar manner to the rib cage, motion of the abdomen can be described by the motion of two subcompartments: the cephalad portion of the abdomen wall is attached to the costal margin and moves when the costal margin moves9,12; the caudal portion of the abdominal wall is not moved by the costal margin. Thus, the cephalad portion is the only part of the abdominal wall that can be pulled outward with an inspiratory action as a result of muscle contraction. But this muscular
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extent that the rib cage resists bending, there will be an interaction between the two rib cage compartments, tending to minimize distortions.14 Although, almost certainly, both rib cage compartments expand, the displacements and distortions between the two rib cage compartments have not yet been studied in detail. Now let us see what happens when the inspiratory muscles of the rib cage contract in isolation. These muscles, of which the most important are the scalene muscles and parasternal muscles,4,5 also include whatever external intercostal muscles are activated during breathing and the sternocleidomastoid muscles. As pointed out above, thesemuscles insert almost exclusively into the pulmonary rib cage. Contracting the inspiratory rib cage muscles therefore has a direct action in expanding the pulmonary rib cage, making Ppl more negative, inflating the lung and sucking the diaphragm in a cephalad direction, passively stretching it. Because the diaphragm is relaxed, the negative Ppl is transmitted to the abdomen, so that Pab falls as well, but not by as much as Ppl, because of the passive Pdi resulting from the stretching of the diaphragmatic fibers. The fall in Pab acts to displace the abdominal wall and the abdominal rib cage inward, whereas the passively stretched costal diaphragmatic fibers tend to expand the abdominal rib cage. The net effect on the abdomen is expiratory, whereas the net effect on the whole chest wall is inspiratory. Hence, the expiratory displacement of the abdominal wall, which equals the cephalad displacement of the diaphragm, is not as great as the inspiratory displacement of the pulmonary rib cage. Again, the effect on the abdominal rib cage is not straightforward, and the precise displacements and distortions have not yet been accurately measured. What happens when the diaphragm, often referred to as the most important respiratory muscle, is the only muscle contracting? The diaphragms connections with the rib cage are all at the costal margin on ribs 7 to 12 in the abdominal rib cage (except for a tiny slip at the bottom of the sternum). Thus, it has only a minimal direct action on the pulmonary rib cage. When it contracts, its fibers exert a force on the central tendon, which is displaced caudally, compressing the abdominal contents, increasing Pab, and displacing the abdominal wall outward.24 At the same time, the fibers originating from the costal margin exert a cephalad force on the abdominal rib cage through ribs 7 to 12, and this is augmented by the increase in Pab acting in the area of apposition of diaphragm to rib cage.15,24 The purpose of diaphragmatic contraction is to develop a pressure difference across the muscle, so that as Pab increases, Ppl decreases, thereby inflating the lung. Thus, the action of the diaphragm on both the abdomen and the lung is purely inspiratory, but the decrease in Ppl has an expiratory effect on the pulmonary rib cage. If the diaphragm contracts against a closed glottis, when, to a close approximation, chest wall and lung volume remain constant, the pulmonary rib cage is displaced inward as the abdomen is displaced outward.20 Whereas the increase in Pab and the tension developed in the costal fibers act to expand the abdominal rib cage, this is almost exactly counterbalanced
by the expiratory displacement of the pulmonary rib cage and the resistance of the rib cage to bending, so that no net movement of the abdominal rib cage occurs, and considerable rib cage distortion takes place.21 The motions occurring when the diaphragm is the only muscle contracting and air is free to flow into the lung have not yet been studied with precision, but it is likely that significant rib cage distortions would also take place. The pulmonary rib cage would be caught between the expiratory force of the fall in Ppl acting over its whole inner surface and the inspiratory action of the expanding abdominal rib cage taking the pulmonary rib cage along with it. As most of the force developed by the diaphragm on the rib cage would go into distorting it, and only a small fraction into expanding it,20 this would be an inefficient way to breathe. Rib cage distortions are costly,20 so a good way to breathe is to avoid them altogether. As discussed above, rib cage distortions are minimal during breathing in normal subjects, even during heavy exercise. Rib cage distortions have not been studied to any significant extent in disease, but in airways obstruction with hyperinflation, one might expect a decrease in the area of apposition, and with extreme hyperinflation, a change in the direction of force exerted by the diaphragm at the costal margin from axial to radial. If this was the case, the diaphragm would tend to deflate the abdominal rib cage, both because this part of the rib cage would now be exposed to the deflationary action of Ppl over the surface of the lung and because of the radial direction of tension in the costal fibers acting at the costal margin.
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Mechanics of Breathing
50 ABM
recruitment of expiratory muscles, even at zero workload.12 The abdominal muscles are the main ones recruited; the expiratory rib cage muscles are recruited to a lesser extent. The expiratory muscles are recruited cyclically, starting at the beginning of expiration and increasing the pressure that they develop throughout expiration, which reaches its maximal value at end-expiration. Then they do not relax right away, but slowly throughout inspiration (Figure 7-1). This results in a Pab that is high at the beginning of inspiration but falls progressively throughout inspiration, in striking contrast to breathing at rest, when Pab increases throughout inspiration.12 The pressures developed by the various respiratory muscle groups during quiet breathing and as a function of exercise workload are shown in Figure 7-2. At rest, only the diaphragm and the inspiratory rib cage muscles are active. At the onset of exercise, even at zero workload, the abdominal and expiratory rib cage muscles are recruited. Surprisingly, Pdi decreases from quiet breathing to zero workload exercise, and as exercise workload increases, Pdi only increases modestly. At zero workload and above, Pabm and Prcm are considerably greater than Pdi.
FIGURE 7-2 Pressures developed by the diaphragm (Di; open triangles), the abdominal muscles (ABM: closed triangles), and the inspiratory and expiratory rib cage muscles (RCMi: open circles; RCMe: closed circles, respectively) during quiet breathing (QB) and during exercise at 0, 30, 50, and 70% maximal exercise workload. Reproduced with permission from Aliverti A et al.17
FIGURE 7-1 Pressure volume diagram of the abdomen during relaxation, quiet breathing, and various levels of exercise. Vab, volume displaced by the abdominal wall. Pga , gastric pressure, used as an index of abdominal pressure (Pab). The straight line with a positive slope at lower values of Vab and bending to the right at high Vab is the relaxation pressure-volume curve of the abdomen and Pabw is the elastic recoil pressure of the abdomen. The heavy curve along the relaxation line ending in the open circle is the abdominal pressure-volume curve during quiet breathing. The curved lines with negative slopes are dynamic abdominal pressure-volume curves during various levels of exercise. The open circle at the bottom end of the largest of these curves is a zero-flow point at end-expiration. The upper open circle is a zero-flow point at end-inspiration. The pressure generated by the abdominal muscles (Pabm) at any Vab is the horizontal distance between the relaxation and dynamic curves at that Vab. Reproduced with permission from Aliverti A et al.17
Evidently, as soon as exercise starts, there is an immediate change in the central drive to the respiratory muscles. This drive activates the muscles to produce power, the product of the flow they generate and the pressure they produce. But how this power is partitioned between flow and pressure is not determined by the central drive; it is a unique function of the load that the muscle acts against. During breathing at rest, Pab rises and Ppl falls throughout inspiration, progressively increasing the load on the diaphragm, because both pressures act to impede diaphragmatic descent. The increase in Pab and decrease in Ppl represent the interaction between the activation of the diaphragm produced by the central drive and the elastic loads of the lung and chest wall that the diaphragm is acting against. For a given degree of activation, as these loads increase during inspiration, more of the central drive to the diaphragm is converted into Pdi and less is converted into flow. Quite the opposite situation pertains during exercise. The decrease in Pab during inspiration shown in Figure 7-1 parallels the decrease in Ppl. If Pab Ppl, then the diaphragm would contract quasi-isotonically, and the elastic loads would disappear. Thus, the gradual relaxation of abdominal muscles throughout inspiration unloads the diaphragm so that more of the central drive is converted to flow and less to pressure. This is illustrated in Figure 7-3, which shows that most of the diaphragms power during exercise is expressed as flow rather than pressure. Indeed, the fold increases in power developed by the inspiratory rib cage muscles, the abdominal muscles, and the diaphragm as a function of exercise workload are all about the same (Figure 7-4). The fact that inspiratory Prcm and Pabm exceed Pdi indicates that the diaphragms role during exercise is primarily as a flow generator, whereas the
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Vdi
. Wdi
12 9 * 6 3 0 QB 0 20 40 60 80 QB 0 20 40 60 80 QB 0 20 40 60 80 * * * * * * * *
. Workload (% Wmax)
inspiratory rib cage and abdominal muscles are primarily pressure generators acting to displace the rib cage and abdomen, respectively. This is shown for the diaphragm and inspiratory rib cage muscles in the lower panel of Figure 7-4, in which the power developed by these muscles is partitioned into its pressure and flow components as the ratio between pressure and velocity of shortening. During exercise, the conditions for no rib cage distortion are the same as in Equation 7-1, except that Pabm is both active and passive. Expressing Equation 7-1 in terms of changes gives: Prcm (x 1) Pdi yPabm (7-2)
FIGURE 7-3 Fold increases over quiet breathing of transdiaphragmatic pressure (left panel), velocity of shortening (middle panel), and power (right panel) developed by the diaphragm as a function of exercise workload. Reproduced with permission from Aliverti A et al.17
Prcm now includes both inspiratory and expiratory rib cage muscles. The condition for both lack of rib cage distortion and isotonic diaphragm contraction is obtained by setting Pdi 0 in Equation 7-2: Prcm yPabm (7-3)
Power
Equation 7-3 states that a simple control system by which the central drive to the combined inspiratory and expiratory rib cage muscles is exactly 180 out of phase with the drive to the abdominal muscles, with a constant of proportionality equal to y, accomplishes two remarkable things: it prevents costly rib cage distortions and removes the elastic load from the diaphragm, allowing it to act as a flow generator.12 The plot of Prcm versus Pabm during exercise is shown in Figure 7-5 and confirms that the pressures developed by these two muscle groups are, in fact, nearly 180 out of phase.12 In addition to preventing rib cage distortions and allowing the diaphragm to act as a flow generator, the
30 Workload (% max) 50 70
QB
40
Pressure/velocity ratio
30
Pabm [cmH2O]
RCMi
70% 20
10
Di
0
QB
QB
30 Workload (% max)
50
70
-10
10 Prcm [cmH2O]
20
30
FIGURE 7-4 Power and its partitioning into pressure and flow during quiet breathing (QB) and as a function of exercise workload. Upper panel: Power developed by the diaphram (open triangles), inspiratory rib cage muscles (open circles), and abdominal muscles (closed triangles); lower panel: partitioning of power of the inspiratory rib cage muscles and the diaphragm. Reproduced with permission from Aliverti A et al.17
FIGURE 7-5 Relationship between the pressures developed by the abdominal muscles (Pabm) and those developed by the rib cage muscles (Prcm) during quiet breathing (QB) and at increasing levels of exercise to a maximum of 70% maximal power output (70%). During all levels of exercise, these pressures are nearly 180 out of phase. Reproduced with permission from Aliverti A et al.17
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1.5
Mechanics of Breathing
Vrc,p Vrc,a Vab
Volume (L)
volume of the abdomen. This stores elastic energy in the respiratory system that can be released during inspiration to perform useful external work. It also lengthens diaphragmatic fibers so that they develop more power for a given level of activation.
REFERENCES
1. De Troyer A, Sampson M, Sigrist S, Macklem PT. The diaphragm: two muscles. Science 1981;213:2378. 2. De Troyer A, Sampson M, Sigrist S, Macklem PT. Action of costal and crural parts of the diaphragm on the rib cage in dog. J Appl Physiol 1982;53:309. 3. De Troyer A, Sampson A, Sigrist S, Kelly S. How the abdominal muscles act on the rib cage. J Appl Physiol 1983;54: 4659. 4. De Troyer A, Estenne M. Coordination between rib cage muscles and diaphragm during quiet breathing in humans. J Appl Physiol 1984;57:899906. 5. Legrand A, Schneider E, Gevenois PA, De Troyer A. Respiratory effects of the scalene and sternomastoid muscles in humans. J Appl Physiol 2003;94:146772. 6. De Troyer A, Kelly S, Macklem PT, Zin WA. Mechanics of intercostal space and actions of external and internal intercostal muscles. J Clin Invest 1985;75:850. 7. Whitelaw WA, Feroah T. Patterns of intercostal muscle activity in humans. J Appl Physiol 1989;67:208794. 8. De Troyer A, Ninane V, Gilmartin JJ, et al. Triangularis sterni muscle use in supine humans. J Appl Physiol 1987;62: 91925. 9. Konno K, Mead J. Measurement of the separate volume changes of rib cage and abdomen during breathing. J Appl Physiol 1967;22:40722. 10. Deschamps C, Rodarte JR, Wilson TA. Coupling between rib cage and abdominal compartments of the relaxed chest wall. J Appl Physiol 1988;65:22659. 11. Mead J, Loring SH. Analysis of volume displacement and length changes of the diaphragm during breathing. J Appl Physiol 1982;53:7505. 12. Aliverti A, Iandelli I, Duranti R, et al. Respiratory muscle dynamics and control during exercise with externally imposed expiratory flow limitation. J Appl Physiol 2002;92:195363. 13. Mead J. Functional significance of the area of apposition of diaphragm to rib cage. Am Rev Respir Dis 1979;119 (2 Pt 2):312. 14. Ward ME, Ward JW, Macklem PT. Analysis of human chest wall motion using a two compartment rib cage model. J Appl Physiol 1992;72:133847. 15. Loring SH, Mead J. Action of the diaphragm on the rib cage inferred from a force-balance analysis. J Appl Physiol 1982;53:75660. 16. Mead J, Loring SH. Analysis of volume displacement and length changes of the diaphragm during breathing. J Appl Physiol 1982;53:7505. 17. Aliverti A, Cala SJ, Duranti R, et al. Human respiratory muscle actions and control during exercise. J Appl Physiol 1997;83:125669. 18. Reid MB, Loring SH, Banzett RB, Mead J. Passive mechanics of upright human chest wall during immersion from hips to neck. J Appl Physiol 1986;60:156170. 19. McCool FD, Loring SH, Mead J. Rib cage distortion during voluntary and involuntary breathing acts. J Appl Physiol 1985;58:170312. 20. Chihara K, Kenyon CM, Macklem PT. Human rib cage distortability. J Appl Physiol 1996;81:43747.
. Workload (% Wmax)
FIGURE 7-6 Volume changes of the lung-apposed rib cage (Vrc,p), the diaphragm-apposed rib cage (Vrc,a), and the abdomen (Vab) during quiet breathing and as a function of exercise workload. On the ordinate, the volumes are referenced to functional residual capacity (FRC) during quiet breathing (0.0). Open circles: endinspiratory volume; closed circles: end-expiratory volume. Reproduced with permission from Aliverti A et al.17
abdominal muscles play another important role: endexpiratory lung volume progressively decreases as exercise workload increases. This allows elastic energy to be stored in the system below FRC that can be released to perform useful external work during inspiration. Furthermore, the reduction in end-expiratory lung volume is entirely accomplished by a reduction in the volume of the abdominal compartment; there is no decrease in the volume of the rib cage at end-expiration, whereas all the increase in lung volume takes place in the rib cage compartment. This is shown in Figure 7-6. As the volume of the abdomen is the main determinant of diaphragmatic fiber length,25 its inward displacement lengthens the diaphragm fibers, allowing it to generate more power for a given degree of central activation.
Act of Breathing: The Ventilatory Pump 21. Kenyon CM, Cala SJ, Yan S, et al. Rib cage mechanics during quiet breathing and exercise in humans. J Appl Physiol 1997;83:124255. 22. De Troyer A. Mechanical role of the abdominal muscles in relation to posture. Respir Physiol 1983;53:34153. 23. Loring SH, Mead J. Abdominal muscle use during quiet breathing and hyperpnea in uninformed subjects. J Appl Physiol 1982;52:7004.
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24. Macklem PT, Macklem DM, De Troyer A. A model of inspiratory muscle mechanics. J Appl Physiol 1983; 55:54757. 25. Aliverti A, Ghidoli G, Dellaca RL, et al. Chest wall kinematic determinants of diaphragm length by optoelectronic plethysmography and ultrasonography. J Appl Physiol 2003;94:62130.